CB1 receptor signaling regulates social anxiety and memory

Genes, Brain and Behavior

Volumn 12, Issue 5, 2013, Pages 479-489

  Litvin, Y ^a,b   Phan, A ^a   Hill, M N ^b   Pfaff, D W ^a   Mcewen, B S ^b  

^a Lab of Hum Behavior and Metabolism   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Behavior; Discrimination; Endocannabinoid; Fear; Interaction; Stress

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; CNR1 PROTEIN, MOUSE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; AROUSAL; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; COPING BEHAVIOR; DEFENSIVE BEHAVIOR; FREEZING; LOCOMOTION; MALE; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; SOCIAL BEHAVIOR; SOCIAL DISCRIMINATION; SOCIAL PHOBIA; WILD TYPE; ADAPTIVE BEHAVIOR; ANIMAL; ANTAGONISTS AND INHIBITORS; ANXIETY; C57BL MOUSE; CATALEPSY; GENETICS; KNOCKOUT MOUSE; METABOLISM; DRUG ANTAGONISM;

ANIMALIA;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; ANXIETY; AROUSAL; FREEZING REACTION, CATALEPTIC; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; SOCIAL DISCRIMINATION;

EID: 84879605567     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12045     Document Type: Article

References (73)

1. Atsak, P., Roozendaal, B. & Campolongo, P. (2012) Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences. Neuroscience 204, 104-116.
2. Azad, S.C., Monory, K., Marsicano, G., Cravatt, B.F., Lutz, B., Zieglgansberger, W. & Rammes, G. (2004) Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24, 9953-9961.
3. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W. & Nestler, E.J. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868.
4. Blanchard, D.C., Spencer, R.L., Weiss, S.M., Blanchard, R.J., McEwen, B. & Sakai, R.R. (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20, 117-134.
5. Buckner, J.D., Mallott, M.A., Schmidt, N.B. & Taylor, J. (2006a) Peer influence and gender differences in problematic cannabis use among individuals with social anxiety. J Anxiety Disord 20, 1087-1102.
6. Buckner, J.D., Schmidt, N.B., Bobadilla, L. & Taylor, J. (2006b) Social anxiety and problematic cannabis use: evaluating the moderating role of stress reactivity and perceived coping. Behav Res Ther 44, 1007-1015.
7. Buckner, J.D., Schmidt, N.B., Lang, A.R., Small, J.W., Schlauch, R.C. & Lewinsohn, P.M. (2008) Specificity of social anxiety disorder as a risk factor for alcohol and cannabis dependence. J Psychiatr Res 42, 230-239.
8. Buckner, J.D., Crosby, R.D., Wonderlich, S.A. & Schmidt, N.B. (2012a) Social anxiety and cannabis use: an analysis from ecological momentary assessment. J Anxiety Disord 26, 297-304.
9. Buckner, J.D., Ecker, A.H. & Vinci, C. (2012b) Cannabis use vulnerability among socially anxious users: cannabis craving during a social interaction. Psychol Addict Behav 1, 236-242.
10. Buckner, J.D., Heimberg, R.G., Schneier, F.R., Liu, S.M., Wang, S. & Blanco, C. (2012c) The relationship between cannabis use disorders and social anxiety disorder in the National Epidemiological Study of Alcohol and Related Conditions (NESARC). Drug Alcohol Depend 124, 128-134.
11. Buckner, J.D., Zvolensky, M.J. & Schmidt, N.B. (2012d) Cannabis-related impairment and social anxiety: the roles of gender and cannabis use motives. Addict Behav 37, 1294-1297.
12. Campolongo, P., Ratano, P., Manduca, A., Scattoni, M.L., Palmery, M., Trezza, V. & Cuomo, V. (2012) The endocannabinoid transport inhibitor AM404 differentially modulates recognition memory in rats depending on environmental aversiveness. Front Behav Neurosci 6, 11.
13. Carter, C.S. & Altemus, M. (1997) Integrative functions of lactational hormones in social behavior and stress management. Ann N Y Acad Sci 807, 164-174.
14. Chakrabarti, B. & Baron-Cohen, S. (2011) Variation in the human cannabinoid receptor CNR1 gene modulates gaze duration for happy faces. Mol Autism 2, 10.
15. Chakrabarti, B., Kent, L., Suckling, J., Bullmore, E. & Baron-Cohen, S. (2006) Variations in the human cannabinoid receptor (CNR1) gene modulate striatal responses to happy faces. Eur J Neurosci 23, 1944-1948.
16. Choleris, E., Ogawa, S., Kavaliers, M., Gustafsson, J.A., Korach, K.S., Muglia, L.J. & Pfaff, D.W. (2006) Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5, 528-539.
17. Degroot, A. & Nomikos, G.G. (2004) Genetic deletion and pharmacological blockade of CB1 receptors modulates anxiety in the shock-probe burying test. Eur J Neurosci 20, 1059-1064.
18. Domschke, K., Dannlowski, U., Ohrmann, P., Lawford, B., Bauer, J., Kugel, H., Heindel, W., Young, R., Morris, P., Arolt, V., Deckert, J., Suslow, T. & Baune, B.T. (2008) Cannabinoid receptor 1 (CNR1) gene: impact on antidepressant treatment response and emotion processing in major depression. Eur Neuropsychopharmacol 18, 751-759.
19. Donaldson, Z.R. & Young, L.J. (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904.
20. Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A. & Chen, A. (2010) Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 13, 1351-1353.
21. Gabor, C.S., Phan, A., Clipperton-Allen, A.E., Kavaliers, M. & Choleris, E. (2012) Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neurosci 126, 97-109.
22. Haller, J., Varga, B., Ledent, C., Barna, I. & Freund, T.F. (2004) Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice. Eur J Neurosci 19, 1906-1912.
23. Haring, M., Kaiser, N., Monory, K. & Lutz, B. (2011) Circuit specific functions of cannabinoid CB1 receptor in the balance of investigatory drive and exploration. PLoS One 6, e26617.
24. Hariri, A.R., Gorka, A., Hyde, L.W., Kimak, M., Halder, I., Ducci, F., Ferrell, R.E., Goldman, D. & Manuck, S.B. (2009) Divergent effects of genetic variation in endocannabinoid signaling on human threat- and reward-related brain function. Biol Psychiatry 66, 9-16.
25. Hill, M.N. & McEwen, B.S. (2010) Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry 34, 791-797.
26. Hill, M.N., McLaughlin, R.J., Bingham, B., Shrestha, L., Lee, T.T., Gray, J.M., Hillard, C.J., Gorzalka, B.B. & Viau, V. (2010a) Endogenous cannabinoid signaling is essential for stress adaptation. Proc Natl Acad Sci U S A 107, 9406-9411.
27. Hill, M.N., Patel, S., Campolongo, P., Tasker, J.G., Wotjak, C.T. & Bains, J.S. (2010b) Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. J Neurosci 30, 14980-14986.
28. Hill, M.N., Kumar, S.A., Filipski, S.B., Iverson, M., Stuhr, K.L., Keith, J.M., Cravatt, B.F., Hillard, C.J., Chattarji, S. & Mcewen, B.S. (2012) Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure. Mol Psychiatry, in press.
29. Howlett, A.C., Barth, F., Bonner, T.I., Cabral, G., Casellas, P., Devane, W.A., Felder, C.C., Herkenham, M., Mackie, K., Martin, B.R., Mechoulam, R. & Pertwee, R.G. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54, 161-202.
30. Jacob, W., Marsch, R., Marsicano, G., Lutz, B. & Wotjak, C.T. (2012) Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo. Neurobiol Learn Mem 98, 47-55.
31. Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Di Marzo, V., Lutz, B. & Wotjak, C.T. (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26, 6677-6686.
32. Kamprath, K., Plendl, W., Marsicano, G., Deussing, J.M., Wurst, W., Lutz, B. & Wotjak, C.T. (2009) Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling. Genes Brain Behav 8, 203-211.
33. Kamprath, K., Romo-Parra, H., Haring, M., Gaburro, S., Doengi, M., Lutz, B. & Pape, H.C. (2011) Short-term adaptation of conditioned fear responses through endocannabinoid signaling in the central amygdala. Neuropsychopharmacology 36, 652-663.
34. Katona, I. & Freund, T.F. (2012) Multiple functions of endocannabinoid signaling in the brain. Annu Rev Neurosci 35, 529-558.
35. Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N. & Freund, T.F. (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21, 9506-9518.
36. Katona, I., Urban, G.M., Wallace, M., Ledent, C., Jung, K.M., Piomelli, D., Mackie, K. & Freund, T.F. (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26, 5628-5637.
37. Klugmann, M., Goepfrich, A., Friemel, C.M. & Schneider, M. (2012) AAV-mediated overexpression of the CB1 receptor in the mPFC of adult rats alters cognitive flexibility, social behavior, and emotional reactivity. Front Behav Neurosci 5, 37.
38. Kodirov, S.A., Jasiewicz, J., Amirmahani, P., Psyrakis, D., Bonni, K., Wehrmeister, M. & Lutz, B. (2009) Endogenous cannabinoids trigger the depolarization-induced suppression of excitation in the lateral amygdala. Learn Mem 17, 43-49.
39. Krebs-Kraft, D.L., Hill, M.N., Hillard, C.J. & McCarthy, M.M. (2010) Sex difference in cell proliferation in developing rat amygdala mediated by endocannabinoids has implications for social behavior. Proc Natl Acad Sci U S A 107, 20535-20540.
40. Krishnan, V., Han, M.H., Graham, D.L. et al. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
41. Kudryavtseva, N.N. (2003) Use of the "partition" test in behavioral and pharmacological experiments. Neurosci Behav Physiol 33, 461-471.
42. Lafenetre, P., Chaouloff, F. & Marsicano, G. (2007) The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 56, 367-381.
43. Litvin, Y., Blanchard, D.C. & Blanchard, R.J. (2007) Rat 22kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182, 166-172.
44. Litvin, Y., Murakami, G. & Pfaff, D.W. (2011) Effects of chronic social defeat on behavioral and neural correlates of sociality: vasopressin, oxytocin and the vasopressinergic V1b receptor. Physiol Behav 103, 393-403.
45. Maccarrone, M., Valverde, O., Barbaccia, M.L., Castane, A., Maldonado, R., Ledent, C., Parmentier, M. & Finazzi-Agro, A. (2002) Age-related changes of anandamide metabolism in CB1 cannabinoid receptor knockout mice: correlation with behaviour. Eur J Neurosci 15, 1178-1186.
46. Marsicano, G. & Lutz, B. (2006) Neuromodulatory functions of the endocannabinoid system. J Endocrinol Invest 29, 27-46.
47. Marsicano, G. & Lafenetre, P. (2009) Roles of the endocannabinoid system in learning and memory. Curr Top Behav Neurosci 1, 201-230.
48. Marsicano, G., Wotjak, C.T., Azad, S.C., Bisogno, T., Rammes, G., Cascio, M.G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V. & Lutz, B. (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530-534.
49. Martin, M., Ledent, C., Parmentier, M., Maldonado, R. & Valverde, O. (2002) Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl) 159, 379-387.
50. McIntyre, C.K., McGaugh, J.L. & Williams, C.L. (2012) Interacting brain systems modulate memory consolidation. Neurosci Biobehav Rev 36, 1750-1762.
51. Metna-Laurent, M., Soria-Gomez, E., Verrier, D., Conforzi, M., Jego, P., Lafenetre, P. & Marsicano, G. (2012) Bimodal control of fear-coping strategies by CB(1) cannabinoid receptors. J Neurosci 32, 7109-7118.
52. Murakami, G., Hunter, R.G., Fontaine, C., Ribeiro, A. & Pfaff, D. (2011) Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice. Eur J Neurosci 34, 469-477.
53. Naderi, N., Haghparast, A., Saber-Tehrani, A., Rezaii, N., Alizadeh, A.M., Khani, A. & Motamedi, F. (2008) Interaction between cannabinoid compounds and diazepam on anxiety-like behaviour of mice. Pharmacol Biochem Behav 89, 64-75.
54. Newsom, R.J., Osterlund, C., Masini, C.V., Day, H.E., Spencer, R.L. & Campeau, S. (2012) Cannabinoid receptor type 1 antagonism significantly modulates basal and loud noise induced neural and hypothalamic-pituitary-adrenal axis responses in male Sprague-Dawley rats. Neuroscience 204, 64-73.
55. Patel, S. & Hillard, C.J. (2008) Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation. Eur J Neurosci 27, 2821-2829.
56. Patel, S., Cravatt, B.F. & Hillard, C.J. (2005) Synergistic interactions between cannabinoids and environmental stress in the activation of the central amygdala. Neuropsychopharmacology 30, 497-507.
57. Pfaff, D.W. (1999) Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation. The MIT Press, Cambridge, MA.
58. Phan, K.L., Angstadt, M., Golden, J., Onyewuenyi, I., Popovska, A. & De Wit, H. (2008) Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. J Neurosci 28, 2313-2319.
59. Phan, A., Lancaster, K.E., Armstrong, J.N., Maclusky, N.J. & Choleris, E. (2011) Rapid effects of estrogen receptor alpha and beta selective agonists on learning and dendritic spines in female mice. Endocrinology 152, 1492-1502.
60. Reibaud, M., Obinu, M.C., Ledent, C., Parmentier, M., Bohme, G.A. & Imperato, A. (1999) Enhancement of memory in cannabinoid CB1 receptor knock-out mice. Eur J Pharmacol 379, R1-R2.
61. Riebe, C.J. & Wotjak, C.T. (2011) Endocannabinoids and stress. Stress 14, 384-397.
62. Riebe, C.J., Pamplona, F.A., Kamprath, K. & Wotjak, C.T. (2012) Fear relief-toward a new conceptual frame work and what endocannabinoids gotta do with it. Neuroscience 204, 159-185.
63. Rodgers, R.J., Evans, P.M. & Murphy, A. (2005) Anxiogenic profile of AM-251, a selective cannabinoid CB1 receptor antagonist, in plus-maze-naive and plus-maze-experienced mice. Behav Pharmacol 16, 405-413.
64. Sink, K.S., Segovia, K.N., Sink, J., Randall, P.A., Collins, L.E., Correa, M., Markus, E.J., Vemuri, V.K., Makriyannis, A. & Salamone, J.D. (2010) Potential anxiogenic effects of cannabinoid CB1 receptor antagonists/inverse agonists in rats: comparisons between AM4113, AM251, and the benzodiazepine inverse agonist FG-7142. Eur Neuropsychopharmacol 20, 112-122.
65. Srivastava, R. K. & Lutz, B. 2012. Dysregulation of hypothalamic-pituitary-adrenal axis in mice lacking CB1 receptor in adrenergic and noradrenergic neurons. In 22nd Annual Symposium of the International Cannabinoid Research Society. Freiburg, Germany.
66. Steiner, M.A. & Wotjak, C.T. (2008) Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis. Prog Brain Res 170, 397-432.
67. Tallett, A.J., Blundell, J.E. & Rodgers, R.J. (2007) Grooming, scratching and feeding: role of response competition in acute anorectic response to rimonabant in male rats. Psychopharmacology (Berl) 195, 27-39.
68. Tallett, A.J., Blundell, J.E. & Rodgers, R.J. (2008) Endogenous opioids and cannabinoids: system interactions in the regulation of appetite, grooming and scratching. Physiol Behav 94, 422-431.
69. Terranova, J.P., Storme, J.J., Lafon, N., Perio, A., Rinaldi-Carmona, M., Le Fur, G. & Soubrie, P. (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berl) 126, 165-172.
70. Terzian, A.L., Drago, F., Wotjak, C.T. & Micale, V. (2011) The dopamine and cannabinoid interaction in the modulation of emotions and cognition: assessing the role of cannabinoid CB1 receptor in neurons expressing dopamine D1 receptors. Front Behav Neurosci 5, 49.
71. Tzavara, E.T., Davis, R.J., Perry, K.W., Li, X., Salhoff, C., Bymaster, F.P., Witkin, J.M. & Nomikos, G.G. (2003) The CB1 receptor antagonist SR141716A selectively increases monoaminergic neurotransmission in the medial prefrontal cortex: implications for therapeutic actions. Br J Pharmacol 138, 544-553.
72. Wilson, R.I. & Nicoll, R.A. (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
73. Zimmer, A., Zimmer, A.M., Hohmann, A.G., Herkenham, M. & Bonner, T.I. (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci U S A 96, 5780-5785.